On the organization of receptive fields of retinal spot detectors projecting to the fish tectum: Analogies with the local edge detectors in frogs and mammals

• Published in: Journal of comparative neurology (1911) Vol. 528; no. 8; pp. 1423 - 1435
• Main Authors: Maximova, Elena M., Aliper, Alexey T., Damjanović, Ilija, Zaichikova, Alisa A., Maximov, Paul V.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01-06-2020; Wiley Subscription Services, Inc
• Subjects: extracellular recording; Firing pattern; fish; Ganglion cells; Motion detection; Orientation behavior; Presynapse; Retina; retinotectal projections; Sensors; spot detectors; Tectum; tectum opticum; Visual field; extracellular recording; ganglion cells; retina; fish; retinotectal projections; tectum opticum; spot detectors
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.24824

Responses of ON‐ and OFF‐ganglion cells (GCs) were recorded extracellularly from their axon terminals in the medial sublamina of tectal retino‐recipient layer of immobilized cyprinid fish (goldfish and carp). These units were recorded deeper than direction selective (DS) ones and at the same depth where responses of orientation selective (OS) GCs were recorded. Prominent responses of these units are evoked by small contrast spots flickering within or moving across their visual field. They are not selective either to the direction of motion or to the orientation of stimuli and are not characterized by any spontaneous spike activity. We refer to these fish GCs as spot detectors (SDs) by analogy with the frog SD. Receptive fields (RFs) of SDs are organized concentrically: the excitatory center (about 4.5°) is surrounded by opponent periphery. Study of interactions in the RF has shown that inhibitory influences are generated already inside the central RF area. This fact suggests that RFs of SDs cannot be defined as homogeneous sensory zone driven by a linear mechanism of response generation. Physiological properties of fish SDs are compared with the properties of frog SDs and analogous mammalian retinal GCs—local edge detectors (LEDs). The potential role of the SDs in visually guided fish behavior is discussed.
Responses of ON‐ and OFF‐ganglion cells (GCs) referred to as spot detectors (SDs) were recorded extracellularly from their axon terminals in the medial sublaminae of tectal retino‐recipient layer of immobilized cyprinid fish. Computer‐generated visual stimuli (contrast edges or spots) were presented on the computer‐controlled CRT monitor to the fish right eye. Stimuli were presented in the limited area of the monitor screen—a square of approximately 11°. Visual responses are recorded from a contralateral lobe of the tectum opticum. Characteristic feature of SDs is prolonged response to small stationary spot, lasting for seconds. We investigated spatial properties of SD receptive fields (RFs). RFs of the recorded units were mapped by the canonical method with a flickering contrast spot (“random checkerboard”). Small spots were flashed on and off sequentially in nodes of square grid in a quasi‐random order and evoked responses were counted. Cell responses over the entire stimulation area are represented in the form of topographic map. Lateral interactions in the RFs were analyzed by another test which consisted of stimulation by concentric spots of different sizes. The number of spikes in the unit response initially increases with an increase of the stimulus width up to some “optimal size.” And then it starts to decrease, which points at the start of lateral inhibitory influences. Estimation of the RF excitatory area by the second method was significantly lower than that evaluated by random checkerboard, what indicates that inhibitory influences are generated already inside the RF center (blue concentric area marks central inhibitory zone). This fact suggests that RFs of SDs cannot be defined as homogeneous sensory zone driven by a linear mechanism of response generation. Physiological properties of fish SDs are compared with the properties of frog SDs and analogous mammalian retinal GCs—local edge detectors.